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Morphological and Functional Characteristics of Satellite Glial Cells in the Peripheral Nervous System

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Morphological and Functional Characteristics of Satellite Glial Cells in the Peripheral Nervous System ONLINE FIRST This is a provisional PDF only. Copyedited and fully formatted version will be made available soon. ISSN: 0015-5659 e-ISSN: 1644-3284 Morphological and functional characteristics of satellite glial cells in the peripheral nervous system Authors: A. Milosavljević, J. Jančić, A. Mirčić, A. Dožić, J. Boljanović, M. Milisavljević, M. Ćetković DOI: 10.5603/FM.a2020.0141 Article type: Review article Submitted: 2020-07-28 Accepted: 2020-11-12 Published online: 2020-12-05 This article has been peer reviewed and published immediately upon acceptance. It is an open access article, which means that it can be downloaded, printed, and distributed freely, provided the work is properly cited. Articles in "Folia Morphologica" are listed in PubMed. Powered by TCPDF (www.tcpdf.org) Morphological and functional characteristics of satellite glial cells in the peripheral nervous system Running head: Satellite glial cells in peripheral nervous system A. Milosavljević1, J. Jančić2, A. Mirčić1, A. Dožić3, J. Boljanović4, M. Milisavljević4, M. Ćetković1 1Institute of Histology and Embryology, Faculty of Medicine, University of Belgrade, Serbia 2Clinic of Neurology and Psychiatry for Children and Youth, Faculty of Medicine, University of Belgrade, Serbia 3Institute of Anatomy, Faculty of Dental Medicine, University of Belgrade, Serbia 4Laboratory for Vascular Anatomy, Institute of Anatomy, Faculty of Medicine, University of Belgrade, Serbia Address for correspondence: Dr. Mila ĆETKOVIĆ, Institute of Histology and Embryology, Faculty of Medicine, University of Belgrade, Višegradska 26, 11000 Belgrade, Serbia; tel/fax: +381/11/3607-145, e-mail: [email protected] ABSTRACT Satellite glial cells are specialized cells that form a functional perineuronal sheath around sensory ganglion neurons. There are a large number of studies that reveal the morphological and functional characteristics of these cells. Satellite glial cells have been studied both in intact ganglions and in tissue cultures, using light and transmission electron microscopy, immunohistochemical and other methods. Satellite glial cells have polygonal form; they are mononuclear and have developed synthetic organelles, numerous receptors, adhesion molecules and ion channels, which enable them to interact with adjacent neurons, as well as transmit signals in the ganglions of the peripheral nervous system. Based on the literature data, satellite glial cells thanks to their characteristics can receive signals from other cells and react to changes in their surroundings. Previous studies have investigated the potential role of satellite glial cells in the formation of the blood-nervous tissue barrier of the peripheral nervous system, as well as in the neuropathic pain genesis. Some recent discoveries support the fact that satellite glial cells can participate in controlling of local viral infections and protecting pseudounipolar neurons from mentioned infections. Key words: satellite glial cell, sensory ganglion, peripheral nervous system, pseudounipolar neuron INTRODUCTION A large number of scientists are researching the morphology and function of satellite glial cells (SGC) and the number of studies is increasing and increasing. The application of histochemical and electron microscopic methods in satellite glial cell research can contribute to the identification of complex mechanisms of functioning of these cells, as well as their role in numerous diseases of the peripheral nervous system ganglions [29, 38, 44, 50, 58] Satellite glial cells continually envelop neurons in peripheral nervous system ganglions. They completely encircle the ganglionic neurons in the form of one, and rarely two or three concentric layers, and together form morphological and functional units. The extracellular space between them and neurons has a diameter of only 20 nm. Satellite glial cells are small, flattened, and interconnected by gap junctions [47, 49, 50]. The multiplication of satellite glial cells and the formation of several of their layers were registered after the experimental disruption of the axons of the ganglion neurons [17, 41]. The close relationships between satellite and ganglia cells also allow them to communicate with each other. One of the main messengers in this communication is nitrogen monoxide [62, 66]. The protective role of satellite glial cells is also reflected in the secretion of individual neurotrophins, which help the survival of ganglion neurons [66, 74]. MORPHOLOGICAL CHARACTERISTICS OF SATELLITE GLIAL CELLS Short history of satellite glial cells Small perineuronal cells, which form a cell envelope around the body of neurons in sensory ganglions, were first mentioned by Valentine, in 1836 [67]. Even Ramon y Cajal himself named these cells several times [54]. In the late 1950s, the term satellite cell was widely accepted. As the term satellite cells also refers to skeletal muscle fiber progenitor cells, the authors agreed to name them satellite glial cells, with the recommendation that their exact location should be specified (e.g. satellite glial cells of trigeminal ganglion) [50]. Until the discovery of the electron microscope, various controversies arose as to whether the body of each neuron of the sensory ganglion was surrounded by satellite glial cells, since light microscopy has not always shown this in the past [29]. The advent of electron microscopy resolved these disputes, showing that the body of each nerve cell in the sensory ganglion is surrounded by a continuous sheath composed of discrete satellite glial cells [50]. Because the arrangement of satellite glial cells and the thickness of the sheath they build may vary in different areas and in different species, the fact that once these structures were below the resolution of light microscopy explains a different interpretation of the structure of the perineuronal sheath [44, 58]. Along with the development of the electron microscope, the resolution power of the light microscopy has grown, and even today, with light microscopy methods, at different cross-sectional levels, we can clearly see that satellite glial cells completely envelop sensory neurons [29, 38]. Organization of the satellite glial cells in sensory ganglia In sensory ganglions, connective tissue sharply separates satellite glial cells' sheath belonging to one neuron from the sheaths belonging to other neurons (Figs. 1, 2). The outer surface of satellite glial cells, the one facing the interstitial connective tissue, is covered by a basal lamina (Figs. 1A, 1B). This surface is generally flatter than the one facing the neuron. In the peripheral parts of the cytoplasm of satellite glial cells, dense amorphous plaques may also be encountered, whose structure and function are still poorly understood. In the rabbit spinal ganglions, large voids (lacunae) have occasionally been observed, just below the outer surface of the satellite glial cell plasmalemma [49]. It has been observed that cilia and microvilli can be projected into these voids [49]. These lacunar spaces have been observed only in animal models and their significance has not been demonstrated so far [49]. Satellite glial cells have polygonal form; they are mononuclear (Figs. 1C, 1D), and have developed synthetic organelles, numerous receptors, adhesion molecules and ion channels, which allow them to interact with adjacent neurons as well as to transmit signals in the ganglions of the peripheral nervous system [17]. They have very expressed granular endoplasmic reticulum, mitochondria, Golgi apparatus, lysosomes, peroxisomes [18, 20, 43]. The expressed cytoskeletal components are microtubules and intermediate filaments, as well as occasionally present cellular inclusions such as lipofuscin granules [5, 44, 45]. The cell membranes of satellite glial cells differ in thickness from the cell membranes of neurons [50]. In cell membranes of satellite glial cells treated with the freeze-section procedure, sets of orthogonally arranged particles were found [42]. The distance between these particles is about 7 nm [16]. Similar structures have been observed in astrocytes, ependymal cells of higher vertebrates, while they have never been recognized within the cell membranes of oligodendrocytes or neurons [25, 55]. These structures are much rarer in satellite glial cell membranes than in astrocyte membranes [25]. These structures were later shown to be constructed from the aquaporin-4 protein, a membrane protein involved in the transport of water across the cell membrane [55, 69]. Satellite glial cells possess long and branched cytoplasmic extensions, especially on surfaces facing neurons [64]. Because of the large number of cytoplasmic extensions of both neurons and satellite glial cells, it is very difficult to determine precisely the boundary between neurons and satellite glial cells. In the past, these cytoplasmic extensions were thought to be the result of deformation of satellite glial cells due to the use of different procedures [46]. Even after prolonged in vitro cultivation of sensory ganglions, satellite glial cells have been shown to retain shapes similar to those observed in in vivo conditions [5, 64, 73]. Their cytoplasmic extensions may be ring-shaped or may have a lamellar shape [5, 73]. Extensions in cilia are also described in the literature [45]. These cilia lack a central microtubule pair and show only nine pairs of peripheral microtubules, as well as in neurons, in Schwann cells and astrocytes [45]. Finding specific receptors on the solitary cilia of particular neurons supports
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